Review
Impact of recombination on bacterial evolution

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Genetic exchange plays a defining role in the evolution of many bacteria. The recent accumulation of nucleotide sequence data from multiple members of diverse bacterial genera has facilitated comparative studies that have revealed many features of this process. Here we focus on genetic exchange that has involved homologous recombination and illustrate how nucleotide sequence data have furthered our understanding of: (i) the frequency of recombination; (ii) the impact of recombination in different parts of the genome; and (iii) patterns of gene flow within bacterial populations. Summarizing the results obtained for a range of bacteria, we survey evidence indicating that the extent and nature of recombination vary widely among microbiological species and often among lineages assigned to the same microbiological species. These results have important implications in studies ranging from epidemiological investigations to examination of the bacterial species problem.

Section snippets

Recombination in bacteria

Genetic exchange, once thought to be uncommon in asexually reproducing bacteria, is now known to be a major driving force in the evolution of most prokaryotes. Indeed, the lack of genetic exchange among bacteria can now be regarded as an unusual situation, confined to a few lineages such as genetically monomorphic pathogens [1]. Gene transfer among and within bacterial populations is mediated by the three mechanisms of conjugation, transduction and transformation [2]. These processes promote

Rates of recombination

Several different approaches have been used to estimate recombination frequencies in natural populations of bacteria. The rate of recombination relative to that of mutation is a measure often used [10]. A relative rate of recombination of 5, for example, means that recombination has occurred five times as often as mutation during the evolution of the population investigated. Each recombination event is likely to introduce several substitutions, so a relative recombination rate of 1 will usually

Genomic regions affected by recombination

When recombination occurs, a fragment of imported genetic material is integrated in the genome of the recipient. The imported fragment is usually assumed to be contiguous, although two recent laboratory results have shown that this is not always the case after transformation of Helicobacter pylori35, 36. Large recombination events are thought to be rare in nature, although a few have been observed, most of which were probably caused by conjugative gene transfer followed by positive selection.

Patterns of gene flow

Several factors make recombination more likely to occur between closely related bacteria. The first factor is physical proximity, which is required for transformation, transduction or conjugation to take place. This proximity is more likely to occur between members of the same community, which are likely to be related because many species of bacteria show significant geographical and ecological structuring. The geographical structure of H. pylori has been described using the program STRUCTURE (

Concluding remarks and future perspectives

The ever-increasing availability of contiguous nucleotide sequences from multiple regions of bacterial genomes has revealed the central role of homologous recombination in the evolution of most bacterial populations. Clonality now seems to be a special case that relies on extreme genetic isolation associated with very specialized ecologies, especially in obligate pathogens. Sequence data at the population level have led to a better understanding of the nature and rates of recombination in a

Acknowledgments

Xavier Didelot is a CRiSM Research Fellow. Martin Maiden is a Wellcome Trust Senior Fellow. We thank Mark Achtman, Daniel Falush, William Hanage and three anonymous reviewers for providing useful comments, ideas and discussions.

Glossary

Adaptation
evolutionary process whereby a lineage becomes better suited to its environment and potentially less suited to other environments.
Admixture
results from recombination among members of distinct evolutionary lineages.
Ecological structure
non-random association of evolutionary lineages and the ecological niches in which they are found.
Geographical structure
non-random association of evolutionary lineages and the geographical location where they are found.
Lineage
a subgroup of bacteria within

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